Evolutionary variation in cognition

Cognition in the wild: understanding animal thought in its natural context

Rosati, A.G., Machanda, Z.P., & Slocombe, K.E. (2022). Cognition in the wild: understanding animal thought in its natural context. Current Opinion in Behavioral Sciences, 47: 101210.

[PDF] [Publisher’s version] Abstract
Why study cognition in the wild? Comparative perspectives on cognition from nonhumans have long been an important avenue for answering questions about how the mind works, sometimes with animals standing in as models for different aspects of human thought, and sometimes with a focus on the diverse cognitive processes of different species. Yet, research in comparative cognition has to date overwhelmingly involved inquiry based in laboratories. While such captive contexts can allow for the control needed to tease apart the mechanisms underlying behavior, they are also limited in several crucial ways. In particular, understanding cognition requires examining how it works in the real world — which can be messy, complex, and confusing. While cognition may be challenging to study in natural contexts, such data are crucial to fully understand the breadth and depth of nonhuman thought and how it contributes to real-world behavior. Situating cognition in the wild — the context in which it evolved — is therefore necessary to understand the function of these traits.

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The evolution of cognitive control in lemurs

De Petrillo, F., Nair, P., Cantwell, A., & Rosati, A.G. (2022). The evolution of cognitive control in lemurs. Psychological Science, 33: 1408-1422.

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Cognitive control, or executive function, is a key feature of human cognition, allowing individuals to plan, acquire new information, or adopt new strategies when the circumstances change. Yet it is unclear which factors promote the evolution of more sophisticated executive-function abilities such as those possessed by humans. Examining cognitive control in nonhuman primates, our closest relatives, can help to identify these evolutionary processes. Here, we developed a novel battery to experimentally measure multiple aspects of cognitive control in primates: temporal discounting, motor inhibition, short-term memory, reversal learning, novelty responses, and persistence. We tested lemur species with targeted, independent variation in both ecological and social features (ruffed lemurs, Coquerel’s sifakas, ring-tailed lemurs, and mongoose lemurs; N = 39) and found that ecological rather than social characteristics best predicted patterns of cognitive control across these species. This highlights the importance of integrating cognitive data with species’ natural history to understand the origins of complex cognition.

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Insights from matched species comparisons for understanding cognition in the wild

De Petrillo, F., Bettle, R. & Rosati, A.G. (2022). Insights from matched species comparisons for understanding cognition in the wild. Current Opinion in Behavioral Sciences.

[PDF] [Publisher’s version] Abstract

Studies of cognition in the wild are crucial for understanding cognition in natural contexts, but studies of animal cognition in captive populations, living in conditions resembling those of their natural environment, complement this approach and provide new insights into the evolution of cognition. To show how these approaches can work in tandem, we use data from recent comparisons on cognition across different primate species in similar settings. We discuss how this work can disentangle stable species-specific differences in cognition from local environmental effects, distinguish specific cognitive mechanisms supporting behavior, and reveal hidden variables that shape cognition in captivity and the wild. Integration of research in both captive and wild settings will therefore provide a holistic understanding of the origins and function of different cognitive processes.

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Sensitivity to line-of-sight in tolerant versus despotic macaques (Macaca sylvanus and Macaca mulatta)

Bettle, R. & Rosati, A.G. (2022) Sensitivity to line-of-sight in tolerant versus despotic macaques (Macaca sylvanus and Macaca mulatta). Journal of Comparative Psychology, 136: 93–104.

[PDF] [Supplementary] [Study Video] [Publisher’s version] [Commentary] Abstract
Complex social life is considered important to the evolution of cognition in primates. One key aspect of primate social interactions concerns the degree of competition that individuals face in their social group. To examine how social tolerance versus competition shapes social cognition, we experimentally assessed capacities for flexible gaze-following in more tolerant Barbary macaques (Macaca sylvanus) and compared to previous data from despotic rhesus macaques (Macaca mulatta). Monkeys experienced one of two possible conditions. In the barrier condition, they observed an actor look upwards into an overheard barrier, so they could not directly see the target of the actor’s gaze without reorienting. In the no barrier condition, they observed an actor look upwards without a barrier blocking her line-of-sight, so they could observe the target of the actor’s gaze by also looking upwards. Both species (N = 58 Barbary macaques, 64 rhesus macaques) could flexibly modulate their gaze responses to account for the demonstrator’s line of sight, looking up more often when no barrier was present, and this flexible modulation declined with age in both species. However, neither species preferentially approached to look inside the barrier when their view of the target location was obscured, although rhesus macaques approached more overall. This pattern suggests that both tolerant and despotic macaques exhibit similar capacities to track other’s line of sight and do not preferentially reorient their bodies to observe what an actor looks at in this situation. This contrasts with other work indicating that competitive primates are especially adept at some aspects of theory of mind. Thus, it is important to understand both the similarities and differences in the social–cognitive abilities of primates with different social styles.

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The primate origins of human social cognition

Bettle, R. & Rosati, A.G. (2021). The primate origins of human social cognition. Language Learning and Development, 17: 96-127

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The ability to understand the mental states of other individuals is central to human social behavior, yet some theory of mind capacities are shared with other species. Comparisons of theory of mind skills across humans and other primates can provide a critical test of the cognitive prerequisites necessary for different theory of mind skills to emerge. A fundamental difference between humans and non-humans is language: while language may scaffold some developing theory of mind skills in humans, other species do not have similar capacities for or immersion in language. Comparative work can therefore provide a new line of evidence to test the role of language in the emergence of complex social cognition. Here we first provide an overview of the evidence for shared aspects of theory of mind in other primates, and then examine the evidence for apparently human-unique aspects of theory of mind that may be linked to language. We finally contrast different evolutionary processes, such as competition and cooperation, that may have been important for primate social cognition versus human-specific forms of theory of mind. We argue that this evolutionary perspective can help adjudicate between different proposals on the link between human-specific forms of social cognition and language.

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Variation in primate decision-making under uncertainty and the roots of human economic behaviour

De Petrillo, F. & Rosati, A.G. (2021). Variation in primate decision-making under uncertainty and the roots of human economic behaviour. Philosophical Transactions of the Royal Society B, 376: 20190671

[PDF] [Supplementary] [Publisher’s version] Abstract
Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals, and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generates this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here we examine decision-making under risk across primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess current evidence for variation in animal preferences between species and populations; between individuals based on personality, sex, and age; and finally, between different contexts and individual states. We then use this primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour.

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Decision-making in animals: rational choices and adaptive strategies

De Petrillo, F. & Rosati, A.G. (2021). Decision-making in animals: rational choices and adaptive strategies. In: Cambridge Handbook of Animal Cognition (A. Kaufman, J. Call, & J. Kaufman, eds.) Cambridge: Cambridge University Press, pp. 770-791.

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Humans face a myriad of choices every day, from simple decisions about what to eat for lunch or how much time to spend on leisure versus work, to more complex decisions like selecting between competitive jobs offers or deciding whether or not get married. How do we make these choices? This question has spurred research in decision science across fields including economics, psychology, and biology, and has led to the development of several normative theories and models predicting how decision-makers should act to choose optimally.

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Shifting sociality during primate ageing

Machanda, Z.P. & Rosati, A.G. (2020). Shifting sociality during primate ageing. Philosophical Transactions of the Royal Society B, 375: 20190620.

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Humans exhibit major age-related shifts in social relationships along with changes in social and emotional psychological processes that underpin these behavioral shifts. Does social aeging in nonhuman primates follow similar patterns, and if so, what are the ultimate evolutionary consequences of these social shifts? Here we synthesize empirical evidence for shifts in social behavior and underlying psychological processes across species. Focusing on three elements of social behavior and cognition that are important for humans—propensities to engage with others, the positive versus negative valence of these interactions, and capabilities to influence others, we find evidence for wide variation in the trajectories of these characteristics across primates. Based on this, we identify potential modulators of the primate social ageing process, including social organization, sex, and dominance status. Finally, we discuss how comparative research can contextualize human social ageing.

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Logical inferences from visual and auditory information in ruffed lemurs and sifakas

De Petrillo, F. & Rosati, A.G. (2020). Logical inferences from visual and auditory information in ruffed lemurs and sifakas. Animal Behaviour, 164: 193-204

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Inference by exclusion, or the ability to select a correct course of action by systematically excluding other potential alternatives, is a form of logical inference that allow individuals to solve problems without complete information. Current comparative research shows that several bird, mammal, and primate species can find hidden food through inference by exclusion. Yet there is also wide variation in how successful different species are, as well kinds of sensory information they can use to do so. An important question is therefore why some species are better at engaging in logical inference than others. Here, we investigate the evolution of logical reasoning abilities by comparing two strepsirrhine primate species that vary in dietary ecology: frugivorous ruffed lemur (Varecia spp.) and folivorous Coquerel’s sifakas (Propithecus coquereli). Across two studies, we examined their abilities to locate food using direct information versus inference from exclusion and using both visual and auditory information. In Study 1, we assessed whether these lemurs could make inferences when full visual and auditory information about the two potential locations of food were provided. In Study 2, we then compared their ability to make direct inferences versus inferences by exclusion in both the visual and auditory domains. We found that both lemur species can use visual information to find food, but that only ruffed lemurs were also able to use auditory cues, mirroring differences in the complexity of their wild ecology. We further found that, unlike many anthropoid species tested to date, both strepsirrhine species failed to make inferences by exclusion. These results highlight the importance of natural history in understanding the evolution of logical inference, and help reconstruct the deeper phylogeny of primate cognition.

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Ecological rationality: convergent decision-making in apes and capuchins

De Petrillo, F. & Rosati, A.G. (2019). Ecological rationality: convergent decision-making in apes and capuchins. Behavioural Processes, 164: 201-213.

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Humans and other animals appear to defy many principles of economic ‘rationality’ when making decisions. Here, we use an ecological rationality framework to examine patterns of decision-making across species to illu- minate the origins of these strategies. We argue that examples of convergent evolution—the independent emergence of similar traits in species facing similar environments—can provide a crucial test for evolutionary theories of decision-making. We first review theoretical work from evolutionary biology proposing that many economically-puzzling patterns of decision-making may be biologically adaptive when considering the en- vironment in which they are made. We then focus on convergence in ecology, behavior, and cognition of apes and capuchin monkeys as an example of how to apply this ecological framework across species. We review evidence that wild chimpanzees and capuchins, despite being distantly related, both exploit ecological niches characterized by costly extractive foraging and risky hunting behaviors. We then synthesize empirical studies comparing these species’ decision preferences. In fact, both capuchins and chimpanzees exhibit high tolerance for delays in inter-temporal choice tasks, as well as a preference for risky outcomes when making decisions under uncertainty. Moreover, these species exhibit convergent psychological mechanisms for choices, including emotional responses to decision outcomes and sensitivity to social context. Finally, we argue that identifying the evolutionary pressures driving the emergence of specific decision strategies can shed light into the adaptive nature of human economic preferences.

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Heterochrony in chimpanzee and bonobo spatial memory development

Rosati, A.G. (2019). Heterochrony in chimpanzee and bonobo spatial memory development. American Journal of Physical Anthropology, 169: 302-321.

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Objectives: The emergence of human-unique cognitive abilities has been linked to our species’ extended juvenile period. Comparisons of cognitive development across species can provide new insights into the evolutionary mechanisms shaping cognition. This study examined the development of different components of spatial memory, cognitive mechanisms that support complex foraging, by comparing two species with similar life history that vary in wild ecology: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Materials and Methods: Spatial memory development was assessed using a cross-sectional experimental design comparing apes ranging from infancy to adulthood. Study 1 tested 73 sanctuary-living apes on a task examining recall of a single location after a one-week delay, compared to an earlier session. Study 2 tested their ability to recall multiple locations within a complex environment. Study 3 examined a subset of individuals from Study 2 on a motivational control task. Results: In Study 1, younger bonobos and chimpanzees of all ages exhibited improved performance in the test session compared to their initial learning experience. Older bonobos, in contrast, did not exhibit a memory boost in performance after the delay. In Study 2, older chimpanzees exhibited an improved ability to recall multiple locations, whereas bonobos did not exhibit any age-related differences. In Study 3, both species were similarly motivated to search for food in the absence of memory demands. Discussion: These results indicate that closely-related species with similar life history characteristics can exhibit divergent patterns of cognitive development, and suggests a role of socioecological niche in shaping patterns of cognition in Pan.

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Chimpanzee cognition and the roots of the human mind

Rosati, A.G. (2017). Chimpanzee cognition and the roots of the human mind. In: Chimpanzees and Human Evolution (M. Muller, R. Wrangham & D. Pilbeam, eds.). Cambridge: The Belknap Press of Harvard University Press, pp. 703-745.

[PDF] Abstract
The origins of the human mind have been a puzzle ever since Darwin (1871, 1872). Despite striking continuities in the behavior of humans and nonhumans, our species also exhibits a suite of abilities that diverge from the rest of the animal kingdom: we create and utilize complex technology, pass cultural knowledge from generation to generation, and cooperate across numerous and diverse contexts. Why do humans exhibit these abilities, but other animals (mostly) do not? This is a fundamental question in biology, psychology, and philosophy. This puzzle involves two main parts. The first is concerned with identifying the psychological capacities that are unique to humans. This phylogenetic question can be addressed through careful comparisons of humans and other animals to pinpoint the cognitive traits that are likely derived in our species. The second is concerned with the function of these capacities, and the context in which they arose. This evolutionary question examines why, from an ultimate perspective, we evolved these specialized capacities in the first place. Solving these puzzles poses a special challenge because it is only possible to directly measure the cognition of living animals. The bodies of extinct species leave traces in the fossil record, and even some behavioral traits exhibit well-understood relationships with physical traits—such as relationships between dentition and dietary ecology, or mating system and sexual size dimorphism. These relationships provide important benchmarks when biologists infer the behavior of extinct species. Unfortunately, cognition does not fossilize, and neither do the brains that generate cognitive abilities. Even those features of neuroanatomy that do leave some trace in the fossil record—such as brain size or particular anatomical landmarks—are often related to the kinds of complex cognitive capacities potentially unique to humans in a coarse fashion. As such, identifying derived human cognitive traits requires reconstructing the mind of the last common ancestor of chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and humans (Homo sapiens). This reconstruction then can be used to infer what cognitive characteristics have changed in the human lineage.

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Ecological variation in cognition: Insights from bonobos and chimpanzees

Rosati, A.G. (2017). Ecological variation in cognition: Insights from bonobos and chimpanzees. In: Bonobos: Unique in Mind, Brain and Behavior (B. Hare & S. Yamamoto, eds.). Oxford: Oxford University Press, pp. 157-170. 

[PDF] Abstract
Bonobos and chimpanzees are closely related, yet they exhibit important differences in their wild socio-ecology. Whereas bonobos live in environments with less seasonal variation and more access to fallback foods, chimpanzees face more competition over spatially distributed, variable resources. This chapter argues that bonobo and chimpanzee cognition show psychological signatures of their divergent wild ecology. Current evidence shows that despite strong commonalities in many cognitive domains, apes express targeted differences in specific cognitive skills critical for wild foraging behaviours. In particular, bonobos exhibit less accurate spatial memory, reduced levels of patience and greater risk aversion than do chimpanzees. These results have implications for understanding the evolution of human cognition, as studies of apes are a critical tool for modelling the last common ancestor of humans with nonhuman apes. Linking comparative cognition to species’ natural foraging behaviour can begin to address the ultimate reason for why differences in cognition emerge across species.

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Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not

Rosati, A. G., & Santos, L. R. (2017). Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not. Animal Behaviour, 130, 199-207.

[PDF]  [Supplementary]  [Publisher’s Version]  Abstract

Complex social life is thought to be a major driver of complex cognition in primates, but few studies have directly tested the relationship between a given primate species’ social system and their social cognitive skills. We experimentally compared lifespan patterns of a foundational social cognitive skill (following another’s gaze) in tolerant Barbary macaques, Macaca sylvanus, and despotic rhesus macaques, Macaca mulatta. Semi-free-ranging monkeys (N = 80 individuals from each species) followed gaze more in test trials where an actor looked up compared to control trials. However, species differed in ontogenetic trajectories: both exhibited high rates of gaze following as juveniles, but rhesus monkeys exhibited declines in social attention with age, whereas Barbary macaques did not. This pattern indicates that developmental patterns of social attention vary with social tolerance, and that diversity in social behaviour can lead to differences in social cognition across primates.

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Foraging cognition: Reviving the ecological intelligence hypothesis

Rosati, A. G. (2017). Foraging cognition: Reviving the ecological intelligence hypothesis. Trends in Cognitive Sciences, 21, 691-702.

[PDF]  [Publisher’s Version]  Abstract

What are the origins of intelligent behavior? The demands associated with living in complex social groups have been the favored explanation for the evolution of primate cognition in general and human cognition in particular. However, recent comparative research indicates that ecological variation can also shape cognitive abilities. I synthesize the emerging evidence that ‘foraging cognition’ – skills used to exploit food resources, including spatial memory, decision-making, and inhibitory control – varies adaptively across primates. These findings provide a new framework for the evolution of human cognition, given our species’ dependence on costly, high-value food resources. Understanding the origins of the human mind will require an integrative theory accounting for how humans are unique in both our sociality and our ecology.

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